Differential roles of HIC-5 isoforms in the regulation of cell death and myotube formation during myogenesis

Experimental Cell Research

Volumn 313, Issue 19, 2007, Pages 4000-4014

  Gao, Zheng Liang ^a   Deblis, Ryan ^a   Glenn, Honor ^b   Schwartz, Lawrence M ^a,b  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b Pioneer Valley Life Sciences Institute   (United States)

Author keywords

Anoikis; C2C12; Differentiation; Integrin signaling; Satellite cell

Indexed keywords

FIBRONECTIN; ISOPROTEIN; LAMININ; MEMBRANE PROTEIN; PROTEIN HIC 5; PROTEIN HIC 5ALPHA; PROTEIN HIC 5BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL DEATH; CELL DIFFERENTIATION; CELL FUSION; CELL LOSS; CELL SPREADING; CELL SURVIVAL; CONTROLLED STUDY; FOCAL ADHESION; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

EID: 35448941944     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.05.023     Document Type: Article

References (73)

1. Buckingham M., Bajard L., Chang T., Daubas P., Hadchouel J., Meilhac S., Montarras D., Rocancourt D., and Relaix F. The formation of skeletal muscle: from somite to limb. J. Anat. 202 (2003) 59-68
2. Hollway G., and Currie P. Myotome meanderings. Cellular morphogenesis and the making of muscle. EMBO Rep. 4 (2003) 855-860
3. Dhawan J., and Rando T.A. Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol. 15 (2005) 666-673
4. Chen J.C., and Goldhamer D.J. Skeletal muscle stem cells. Reprod. Biol. Endocrinol. 1 (2003) 101
5. 12 murine myoblasts as a model of skeletal muscle development: morpho-functional characterization. Eur. J. Histochem. 48 (2004) 223-233
6. Yaffe D., and Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270 (1977) 725-727
7. Parker M., Seale P., and Rudnicki M. Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nat. Rev., Genet. 4 (2003) 497-507
8. Wei Q., and Paterson B.M. Regulation of MyoD function in the dividing myoblast. FEBS Lett. 490 (2001) 171-178
9. Beauchamp J., Heslop L., Yu D., Tajbakhsh S., Kelly R., Wernig A., Buckingham M., Partridge T., and Zammit P. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 151 (2000) 1221-1234
10. Fujio Y., Guo K., Mano T., Mitsuuchi Y., Testa J.R., and Walsh K. Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol. Cell. Biol. 19 (1999) 5073-5082
11. Wang J., and Walsh K. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 273 (1996) 359-361
12. Shibanuma M., Mashimo J., Kuroki T., and Nose K. Characterization of the TGF beta 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence. J. Biol. Chem. 269 (1994) 26767-26774
13. Fujimoto N., Yeh S., Kang H.Y., Inui S., Chang H.C., Mizokami A., and Chang C. Cloning and characterization of androgen receptor coactivator, ARA55, in human prostate. J. Biol. Chem. 274 (1999) 8316-8321
14. Brown M.C., and Turner C.E. Paxillin: adapting to change. Physiol. Rev. 84 (2004) 1315-1339
15. Carneiro A.M., Ingram S.L., Beaulieu J.M., Sweeney A., Amara S.G., Thomas S.M., Caron M.G., and Torres G.E. The multiple LIM domain-containing adaptor protein Hic-5 synaptically colocalizes and interacts with the dopamine transporter. J. Neurosci. 22 (2002) 7045-7054
16. Hu Y., Cascone P.J., Cheng L., Sun D., Nambu J.R., and Schwartz L.M. Lepidopteran DALP, and its mammalian ortholog HIC-5, function as negative regulators of muscle differentiation. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10218-10223
17. Matsuya M., Sasaki H., Aoto H., Mitaka T., Nagura K., Ohba T., Ishino M., Takahashi S., Suzuki R., and Sasaki T. Cell adhesion kinase beta forms a complex with a new member, Hic-5, of proteins localized at focal adhesions. J. Biol. Chem. 273 (1998) 1003-1014
18. Osada M., Ohmori T., Yatomi Y., Satoh K., Hosogaya S., and Ozaki Y. Involvement of Hic-5 in platelet activation: integrin alphaIIbbeta3-dependent tyrosine phosphorylation and association with proline-rich tyrosine kinase 2. Biochem. J. 355 (2001) 691-697
19. Panetti T.S., Hannah D.F., Avraamides C., Gaughan J.P., Marcinkiewicz C., Huttenlocher A., and Mosher D.F. Extracellular matrix molecules regulate endothelial cell migration stimulated by lysophosphatidic acid. J. Thromb. Haemost. 2 (2004) 1645-1656
20. Thomas S.M., Hagel M., and Turner C.E. Characterization of a focal adhesion protein, Hic-5, that shares extensive homology with paxillin. J. Cell. Sci. 112 Pt 2 (1999) 181-190
21. Yang L., Guerrero J., Hong H., DeFranco D.B., and Stallcup M.R. Interaction of the tau2 transcriptional activation domain of glucocorticoid receptor with a novel steroid receptor coactivator, Hic-5, which localizes to both focal adhesions and the nuclear matrix. Mol. Biol. Cell. 11 (2000) 2007-2018
22. Fujita H., Kamiguchi K., Cho D., Shibanuma M., Morimoto C., and Tachibana K. Interaction of Hic-5, A senescence-related protein, with focal adhesion kinase. J. Biol. Chem. 273 (1998) 26516-26521
23. Liu S., Thomas S.M., Woodside D.G., Rose D.M., Kiosses W.B., Pfaff M., and Ginsberg M.H. Binding of paxillin to alpha4 integrins modifies integrin-dependent biological responses. Nature 402 (1999) 676-681
24. Turner C.E., Brown M.C., Perrotta J.A., Riedy M.C., Nikolopoulos S.N., McDonald A.R., Bagrodia S., Thomas S., and Leventhal P.S. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodeling. J. Cell Biol. 145 (1999) 851-863
25. Hagmann J., Grob M., Welman A., van Willigen G., and Burger M.M. Recruitment of the LIM protein hic-5 to focal contacts of human platelets. J. Cell. Sci. 111 Pt 15 (1998) 2181-2188
26. Shibanuma M., Kim-Kaneyama J.R., Ishino K., Sakamoto N., Hishiki T., Yamaguchi K., Mori K., Mashimo J., and Nose K. Hic-5 communicates between focal adhesions and the nucleus through oxidant-sensitive nuclear export signal. Mol. Biol. Cell. 14 (2003) 1158-1171
27. Nishiya N., Tachibana K., Shibanuma M., Mashimo J.I., and Nose K. Hic-5-reduced cell spreading on fibronectin: competitive effects between paxillin and Hic-5 through interaction with focal adhesion kinase. Mol. Cell. Biol. 21 (2001) 5332-5345
28. 12 myoblasts. Cell Struct. Funct. 27 (2002) 21-27
29. Mashimo J., Shibanuma M., Satoh H., Chida K., and Nose K. Genomic structure and chromosomal mapping of the mouse hic-5 gene that encodes a focal adhesion protein. Gene 249 (2000) 99-103
30. Nikolopoulos S.N., and Turner C.E. Integrin-linked kinase (ILK) binding to paxillin LD1 motif regulates ILK localization to focal adhesions. J. Biol. Chem. 276 (2001) 23499-23505
31. Vande Pol S.B., Brown M.C., and Turner C.E. Association of bovine papillomavirus type 1 E6 oncoprotein with the focal adhesion protein paxillin through a conserved protein interaction motif. Oncogene 16 (1998) 43-52
32. Nikolopoulos S.N., and Turner C.E. Actopaxin, a new focal adhesion protein that binds paxillin LD motifs and actin and regulates cell adhesion. J. Cell Biol. 151 (2000) 1435-1448
33. Mori K., Asakawa M., Hayashi M., Imura M., Ohki T., Hirao E., Kaneyama J.R., Nose K., and Shibanuma M. Oligomerizing potential of a focal adhesion LIM protein Hic-5 organizing a nuclear-cytoplasmic shuttling complex. J. Biol. Chem. (2006)
34. Gao Z., and Schwartz L.M. Identification and analysis of Hic-5/ARA55 isoforms: implications for integrin signaling and steroid hormone action. FEBS Lett. 579 (2005) 5651-5657
35. Schwartz L.M. Insect muscle as a model for programmed cell death. J. Neurobiol. 23 (1992) 1312-1326
36. Fahrbach S.E., Nambu J., and Schwartz L.M. Programmed cell death and remodeling of neuromuscular systems during metamorphosis. In: Gilbert L., Gill S., and Iatrou K. (Eds). Comprehensive Molecular Insect Science vol. 2 (2005) 165-198
37. Cao Y., Zhao Z., Gruszczynska-Biegala J., and Zolkiewska A. Role of metalloprotease disintegrin ADAM12 in determination of quiescent reserve cells during myogenic differentiation in vitro. Mol. Cell. Biol. 23 (2003) 6725-6738
38. Kinsella T.M., and Nolan G.P. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7 (1996) 1405-1413
39. Berkes C.A., and Tapscott S.J. MyoD and the transcriptional control of myogenesis. Semin. Cell Dev. Biol. 16 (2005) 585-595
40. Jockusch B.M., and Rudiger M. Crosstalk between cell adhesion molecules: vinculin as a paradigm for regulation by conformation. Trends Cell Biol. 6 (1996) 311-315
41. Gullberg D., Velling T., Lohikangas L., and Tiger C.F. Integrins during muscle development and in muscular dystrophies. Front. Biosci. 3 (1998) D1039-D1050
42. Lewis M.P., Machell J.R., Hunt N.P., Sinanan A.C., and Tippett H.L. The extracellular matrix of muscle-implications for manipulation of the craniofacial musculature. Eur. J. Oral Sci. 109 (2001) 209-221
43. Blanco-Bose W.E., and Blau H.M. Laminin-induced change in conformation of preexisting alpha7beta1 integrin signals secondary myofiber formation. Dev. Biol. 233 (2001) 148-160
44. McClay D.R., and Ettensohn C.A. Cell adhesion in morphogenesis. Annu. Rev. Cell Biol. 3 (1987) 319-345
45. Raff M.C. Social controls on cell survival and cell death. Nature 356 (1992) 397-400
46. Edelblum K., Yan F., Yamaoka T., and Polk D. Regulation of apoptosis during homeostasis and disease in the intestinal epithelium. Inflamm. Bowel Dis. 12 (2006) 413-424
47. Fadeel B., and Orrenius S. Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease. J. Intern. Med. 258 (2005) 479-517
48. De Arcangelis A.F., and Georges-Labouesse E. Integrin and ECM functions: roles in vertebrate development. Trends Genet. 16 (2000) 389-395
49. Parsons J.T. Focal adhesion kinase: the first ten years. J. Cell. Sci. 116 (2003) 1409-1416
50. Cary L.A., and Guan J.L. Focal adhesion kinase in integrin-mediated signaling. Front. Biosci. 4 (1999) D102-D113
51. Osses N., and Brandan E. ECM is required for skeletal muscle differentiation independently of muscle regulatory factor expression. Am. J. Physiol., Cell Physiol. 282 (2002) C383-C3894
52. Melo F., Carey D.J., and Brandan E. Extracellular matrix is required for skeletal muscle differentiation but not myogenin expression. J. Cell. Biochem. 62 (1996) 227-239
53. Sastry S.K., Lakonishok M., Wu S., Truong T.Q., Huttenlocher A., Turner C.E., and Horwitz A.F. Quantitative changes in integrin and focal adhesion signaling regulate myoblast cell cycle withdrawal. J. Cell Biol. 144 (1999) 1295-1309
54. Sastry S.K., Lakonishok M., Thomas D.A., Muschler J., and Horwitz A.F. Integrin alpha subunit ratios, cytoplasmic domains, and growth factor synergy regulate muscle proliferation and differentiation. J. Cell Biol. 133 (1996) 169-184
55. 12 myoblasts is critically regulated by FAK signaling. Am. J. Physiol., Regul. Integr. Comp. Physiol. 289 (2005) R862-R870
56. Miller M.G., Naruszewicz I., Kumar A.S., Ramlal T., and Hannigan G.E. Integrin-linked kinase is a positive mediator of L6 myoblast differentiation. Biochem. Biophys. Res. Commun. 310 (2003) 796-803
57. Huang Y., Li J., Zhang Y., and Wu C. The roles of integrin-linked kinase in the regulation of myogenic differentiation. J. Cell Biol. 150 (2000) 861-872
58. Miyamoto H., Rahman M., Takatera H., Kang H.Y., Yeh S., Chang H.C., Nishimura K., Fujimoto N., and Chang C. A dominant-negative mutant of androgen receptor coregulator ARA54 inhibits androgen receptor-mediated prostate cancer growth. J. Biol. Chem. 277 (2002) 4609-4617
59. Jia Y., Ransom R.F., Shibanuma M., Liu C., Welsh M.J., and Smoyer W.E. Identification and characterization of hic-5/ARA55 as an hsp27 binding protein. J. Biol. Chem. 276 (2001) 39911-39918
60. West K.A., Zhang H., Brown M.C., Nikolopoulos S.N., Riedy M.C., Horwitz A.F., and Turner C.E. The LD4 motif of paxillin regulates cell spreading and motility through an interaction with paxillin kinase linker (PKL). J. Cell Biol. 154 (2001) 161-176
61. Tumbarello D.A., and Turner C.E. Hic-5 contributes to epithelial-mesenchymal transformation through a RhoA/ROCK-dependent pathway. J. Cell. Physiol. (2007)
62. Guignandon A., Boutahar N., Rattner A., Vico L., and Lafage-Proust M.H. Cyclic strain promotes shuttling of PYK2/Hic-5 complex from focal contacts in osteoblast-like cells. Biochem. Biophys. Res. Commun. 343 (2006) 407-414
63. Meriane M., Roux P., Primig M., Fort P., and Gauthier-Rouviere C. Critical activities of Rac1 and Cdc42Hs in skeletal myogenesis: antagonistic effects of JNK and p38 pathways. Mol. Biol. Cell 11 (2000) 2513-2528
64. Wei L., Zhou W., Croissant J.D., Johansen F.E., Prywes R., Balasubramanyam A., and Schwartz R.J. RhoA signaling via serum response factor plays an obligatory role in myogenic differentiation. J. Biol. Chem. 273 (1998) 30287-30294
65. Bryan B.A., Li D., Wu X., and Liu M. The Rho family of small GTPases: crucial regulators of skeletal myogenesis. Cell. Mol. Life Sci. 62 (2005) 1547-1555
66. Posern G., and Treisman R. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 16 (2006) 588-596
67. Frisch S.M., and Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124 (1994) 619-626
68. Shibanuma M., and Nose K. Forced expression of hic-5, a senescence-related gene, potentiates a differentiation process of RCT-1 cells induced by retinoic acid. Int. J. Biochem. Cell Biol. 30 (1998) 39-45
69. Heitzer M.D., and DeFranco D.B. Mechanism of action of Hic-5/androgen receptor activator 55, a LIM domain-containing nuclear receptor coactivator. Mol. Endocrinol. 20 (2006) 56-64
70. Shibanuma M., Mori K., Kim-Kaneyama J.R., and Nose K. Involvement of FAK and PTP-PEST in the regulation of redox-sensitive nuclear-cytoplasmic shuttling of a LIM protein, Hic-5. Antioxid. Redox Signal. 7 (2005) 335-347
71. Drori S., Girnun G.D., Tou L., Szwaya J.D., Mueller E., Xia K., Shivdasani R.A., and Spiegelman B.M. Hic-5 regulates an epithelial program mediated by PPARgamma. Genes Dev. 19 (2005) 362-375
72. Saelzler M.P., Spackman C.C., Liu Y., Martinez L.C., Harris J.P., and Abe M.K. ERK8 down-regulates transactivation of the glucocorticoid receptor through Hic-5. J. Biol. Chem. 281 (2006) 16821-16832
73. Tumbarello D.A., Brown M.C., Hetey S.E., and Turner C.E. Regulation of paxillin family members during epithelial-mesenchymal transformation: a putative role for paxillin {delta}. J. Cell. Sci. 118 (2005) 4849-4863